Evolution through recurrent allopolyploidization

Hybridization and genome doubling regularly stimulate evolution in flowering plants, most probably starting with their origin. Immediately following a polyploidization and/or a hybridization event, a genome suffers adjustments in organization and function at the genetic and epigenetic level. These alterations shape the adaptive success and evolutionary fate of newly formed lineages. Many "key" genes present in the extant angiosperm genomes are believed to have originated as a result of ancient polyploidizations. Now it is recognized that multiple origins are the rule for most allopolyploids, but the long-term evolutionary significance of recurrent allopolyploid formation is unclear. Iterative allopolyploidy often result in substantially different lineages, and it is interesting how such species can maintain distinctiveness while sharing the same genetic heritage and ploidy level. Here we aim to screen genome-wide natural diversity among ecologically-divergent, sibling allopolyploids in order to identify genes that may drive adaptation to different environments and lead to isolation. By taking advantage of the most recent advances in genomic technologies we will investigate i) the long-term fate of duplicated genes and the mechanisms controlling their activity; ii) the nature and adaptive value of the diversity produced by iterative allopolyploidizations to result in rapid ecological diversification; and iii) the functional relevance of correlations between gene expression and the development of a specific phenotype. We will use a sophisticated model system, represented by ecologically divergent but related species of Dactylorhiza in their native environmental context. In the relatively short evolutionary terms relevant for our model system (most probably formed at or after the last glaciation), the divergence in phenotypes is expected to be mainly due to differences in rates of expression rather than to physical differences in the coding region of the genome. The project will provide one of the most comprehensive studies of natural variation within an allopolyploid group and will lead to an enhanced appreciation of the effects of polyploidy on the evolution of metabolic pathways that are significant to adaptation and speciation. It will help towards understanding how species-specific patterns originate and how gene expression polymorphism evolves as species diversify and spread over the landscape. In our approach we will use inferences regarding selection pressures responsible for the presence of a particular individual/species in a given portion of the environment. Finally, the proposed research has the potential to provide a new perspective on the links between polyploidy and functional diversity and it will contribute toward a better understanding and hence prediction of the spectrum of genetic mechanisms active at the intraspecific (population) level.

Hybridization and whole genome doubling (WGD, or polyploidization) have been central to the evolution of flowering plants, starting with their origin. Many of our plant crops are also polyploids. Immediately following a WGD and/or a hybridization event, a genome suffers adjustments in organization and function at the genetic and epigenetic level, thereby shaping the adaptive success and the evolutionary fate of resulting lineages. This project used ecologically-divergent, sibling Dactylorhiza allopolyploids of different ages to investigate gene expression alterations triggered by the recurrent WGD with the aim to better understand their importance to the ecological properties of polyploids.For this aim we quantitavely sequenced the expressed parts of the genomes of nine individuals, including representatives of polyploids and the two diploid parents that produced them. We generally observe a trend of increased overexpression of genes in the younger polyploid Dactylorhiza traunsteineri in comparison to its older sibling D. majalis, whose transcriptome generally resembles more closely those of the diploid parents. The differential gene expression between the polyploids can be related back to a general parental dominance in opposite directions in the polyploids. The screen for quantitative expression differences between ecologically divergent sibling allopolyploids and their diploid progenitors helps to identify genes that drive adaptation to divergent environments and lead to isolation between these species. Indeed, significantly overexpressed genes in D. traunsteineri as compared to D. majalis include some of ecological relevance.Shortly after the start of the present project, a parallel, significantly enlarged submission by the project leader to the FWF has been awarded as a START grant. According to regulations in place, the present stand-alone project has been early terminated, only six months after its start, and the research plan has been transferred to the START grant. The current report details the results obtained within the six months running period of this stand-alone grant, but this research continues within the framework of the new START project.